Transitional B cells in quiescent SLE: An early checkpoint imprinted by IFN
Systemic lupus (SLE) is characterized by a break of B cell tolerance that plays a central role in disease pathophysiology. An early checkpoint defect occurs at the transitional stage leading to the survival of autoreactive B cells and consequently the production of pathogenic autoantibodies. The mai...
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| Published in | Journal of autoimmunity Vol. 102; pp. 150 - 158 |
|---|---|
| Main Authors | , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
England
Elsevier Ltd
01.08.2019
Elsevier |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Systemic lupus (SLE) is characterized by a break of B cell tolerance that plays a central role in disease pathophysiology. An early checkpoint defect occurs at the transitional stage leading to the survival of autoreactive B cells and consequently the production of pathogenic autoantibodies. The main purpose of our work was to determine whether transitional B cells, as the most immature naïve B cell subset upstream of pathogenic B cells, display specific features compared to healthy non SLE subjects. Through extensive analysis of transitional B cells from untreated or low treated, mostly Caucasian, SLE patients, we demonstrated that transitional (T1 and T2) B cell frequencies were increased in SLE and positively correlated with disease activity. SLE transitional B cells displayed defects in two closely inter-related molecules (i.e. TLR9 defective responses and CD19 downregulation). RNA sequencing of sorted transitional B cells from untreated patients revealed a predominant overexpression of interferon stimulated genes (ISGs) even out of flares. In addition, early transitional B cells from the bone marrow displayed the highest interferon score, reflecting a B cell interferon burden of central origin. Hence, the IFN signature in transitional B cells is not confined to African American SLE patients and exists in quiescent disease since the medullary stage. These results suggest that in SLE these 3 factors (i.e. IFN imprintment, CD19 downregulation and TLR9 responses impairment) could take part at the early transitional B cell stage in B cell tolerance by-pass, ultimately leading in periphery to the expansion of autoantibodies-secreting cells.
•SLE transitional B cells display CD19 downregulation and impaired TLR9 response.•IFN signature exists since the B-cell medullary stage, even out of flares.•IFN signature in transitional B cells is not confined to African American SLE.•IFN score correlates with the increase in peripheral transitional B cells. |
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| AbstractList | Systemic lupus (SLE) is characterized by a break of B cell tolerance that plays a central role in disease pathophysiology. An early checkpoint defect occurs at the transitional stage leading to the survival of autoreactive B cells and consequently the production of pathogenic autoantibodies. The main purpose of our work was to determine whether transitional B cells, as the most immature naïve B cell subset upstream of pathogenic B cells, display specific features compared to healthy non SLE subjects. Through extensive analysis of transitional B cells from untreated or low treated, mostly Caucasian, SLE patients, we demonstrated that transitional (T1 and T2) B cell frequencies were increased in SLE and positively correlated with disease activity. SLE transitional B cells displayed defects in two closely inter-related molecules (i.e. TLR9 defective responses and CD19 downregulation). RNA sequencing of sorted transitional B cells from untreated patients revealed a predominant overexpression of interferon stimulated genes (ISGs) even out of flares. In addition, early transitional B cells from the bone marrow displayed the highest interferon score, reflecting a B cell interferon burden of central origin. Hence, the IFN signature in transitional B cells is not confined to African American SLE patients and exists in quiescent disease since the medullary stage. These results suggest that in SLE these 3 factors (i.e. IFN imprintment, CD19 downregulation and TLR9 responses impairment) could take part at the early transitional B cell stage in B cell tolerance by-pass, ultimately leading in periphery to the expansion of autoantibodies-secreting cells. Systemic lupus (SLE) is characterized by a break of B cell tolerance that plays a central role in disease pathophysiology. An early checkpoint defect occurs at the transitional stage leading to the survival of autoreactive B cells and consequently the production of pathogenic autoantibodies. The main purpose of our work was to determine whether transitional B cells, as the most immature naïve B cell subset upstream of pathogenic B cells, display specific features compared to healthy non SLE subjects. Through extensive analysis of transitional B cells from untreated or low treated, mostly Caucasian, SLE patients, we demonstrated that transitional (T1 and T2) B cell frequencies were increased in SLE and positively correlated with disease activity. SLE transitional B cells displayed defects in two closely inter-related molecules (i.e. TLR9 defective responses and CD19 downregulation). RNA sequencing of sorted transitional B cells from untreated patients revealed a predominant overexpression of interferon stimulated genes (ISGs) even out of flares. In addition, early transitional B cells from the bone marrow displayed the highest interferon score, reflecting a B cell interferon burden of central origin. Hence, the IFN signature in transitional B cells is not confined to African American SLE patients and exists in quiescent disease since the medullary stage. These results suggest that in SLE these 3 factors (i.e. IFN imprintment, CD19 downregulation and TLR9 responses impairment) could take part at the early transitional B cell stage in B cell tolerance by-pass, ultimately leading in periphery to the expansion of autoantibodies-secreting cells.Systemic lupus (SLE) is characterized by a break of B cell tolerance that plays a central role in disease pathophysiology. An early checkpoint defect occurs at the transitional stage leading to the survival of autoreactive B cells and consequently the production of pathogenic autoantibodies. The main purpose of our work was to determine whether transitional B cells, as the most immature naïve B cell subset upstream of pathogenic B cells, display specific features compared to healthy non SLE subjects. Through extensive analysis of transitional B cells from untreated or low treated, mostly Caucasian, SLE patients, we demonstrated that transitional (T1 and T2) B cell frequencies were increased in SLE and positively correlated with disease activity. SLE transitional B cells displayed defects in two closely inter-related molecules (i.e. TLR9 defective responses and CD19 downregulation). RNA sequencing of sorted transitional B cells from untreated patients revealed a predominant overexpression of interferon stimulated genes (ISGs) even out of flares. In addition, early transitional B cells from the bone marrow displayed the highest interferon score, reflecting a B cell interferon burden of central origin. Hence, the IFN signature in transitional B cells is not confined to African American SLE patients and exists in quiescent disease since the medullary stage. These results suggest that in SLE these 3 factors (i.e. IFN imprintment, CD19 downregulation and TLR9 responses impairment) could take part at the early transitional B cell stage in B cell tolerance by-pass, ultimately leading in periphery to the expansion of autoantibodies-secreting cells. Systemic lupus (SLE) is characterized by a break of B cell tolerance that plays a central role in disease pathophysiology. An early checkpoint defect occurs at the transitional stage leading to the survival of autoreactive B cells and consequently the production of pathogenic autoantibodies. The main purpose of our work was to determine whether transitional B cells, as the most immature naïve B cell subset upstream of pathogenic B cells, display specific features compared to healthy non SLE subjects. Through extensive analysis of transitional B cells from untreated or low treated, mostly Caucasian, SLE patients, we demonstrated that transitional (T1 and T2) B cell frequencies were increased in SLE and positively correlated with disease activity. SLE transitional B cells displayed defects in two closely inter-related molecules (i.e. TLR9 defective responses and CD19 downregulation). RNA sequencing of sorted transitional B cells from untreated patients revealed a predominant overexpression of interferon stimulated genes (ISGs) even out of flares. In addition, early transitional B cells from the bone marrow displayed the highest interferon score, reflecting a B cell interferon burden of central origin. Hence, the IFN signature in transitional B cells is not confined to African American SLE patients and exists in quiescent disease since the medullary stage. These results suggest that in SLE these 3 factors (i.e. IFN imprintment, CD19 downregulation and TLR9 responses impairment) could take part at the early transitional B cell stage in B cell tolerance by-pass, ultimately leading in periphery to the expansion of autoantibodies-secreting cells. •SLE transitional B cells display CD19 downregulation and impaired TLR9 response.•IFN signature exists since the B-cell medullary stage, even out of flares.•IFN signature in transitional B cells is not confined to African American SLE.•IFN score correlates with the increase in peripheral transitional B cells. |
| Author | Korganow, Anne-Sophie Meffre, Eric Martin, Thierry Gies, Vincent Soulas-Sprauel, Pauline Anolik, Jennifer H. Bird, Anna K. Douiri, Nawal Poindron, Vincent Dieudonné, Yannick Keime, Céline Guffroy, Aurélien Liesveld, Jane Barnas, Jennifer L. |
| AuthorAffiliation | c Laboratoire d’ImmunoRhumatologie Moléculaire, INSERM UMR - S1109, Faculté de Médecine, Fédération Hospitalo-Universitaire OMICARE, Fédération de Médecine Translationnelle de Strasbourg (FMTS), Université de Strasbourg, Strasbourg, France h Blood and Marrow Stem Cell Transplant Program, Department of Internal Medicine and The James P. Wilmot Cancer Center, University of Rochester, New York 14642, USA e UFR Médecine, Université de Strasbourg, Strasbourg, France f IGBMC (Institut de Génétique et de Biologie Moléculaire et Cellulaire), INSERM, U1258, CNRS, UMR7104, Université de Strasbourg, Illkirch, France a CNRS UPR 3572 “Immunopathology and Therapeutic Chemistry”/Laboratory of Excellence Medalis, Institute of Molecular and Cellular Biology (IBMC), Strasbourg, France d Service d’Immunologie Biologique, Pôle de Biologie, Hôpitaux Universitaires de Strasbourg, Strasbourg, France j UFR Sciences pharmaceutiques, Université de Strasbourg, Illkirch-Graffenstaden, France k Departement of Immunobiolo |
| AuthorAffiliation_xml | – name: d Service d’Immunologie Biologique, Pôle de Biologie, Hôpitaux Universitaires de Strasbourg, Strasbourg, France – name: i Department of Infectious Diseases, Hôpitaux Universitaires de Strasbourg, Strasbourg, France – name: e UFR Médecine, Université de Strasbourg, Strasbourg, France – name: k Departement of Immunobiology, Yale University School of Medicine, New Haven, Connecticut, USA – name: a CNRS UPR 3572 “Immunopathology and Therapeutic Chemistry”/Laboratory of Excellence Medalis, Institute of Molecular and Cellular Biology (IBMC), Strasbourg, France – name: g Department of Medicine, Division of Allergy, Immunology and Rheumatology, University of Rochester Medical Center, Rochester, New York, 14642, USA – name: f IGBMC (Institut de Génétique et de Biologie Moléculaire et Cellulaire), INSERM, U1258, CNRS, UMR7104, Université de Strasbourg, Illkirch, France – name: b Department of Clinical Immunology and Internal Medicine, National Reference Center for Autoimmune Diseases, Hôpitaux Universitaires de Strasbourg, Strasbourg, France – name: j UFR Sciences pharmaceutiques, Université de Strasbourg, Illkirch-Graffenstaden, France – name: c Laboratoire d’ImmunoRhumatologie Moléculaire, INSERM UMR - S1109, Faculté de Médecine, Fédération Hospitalo-Universitaire OMICARE, Fédération de Médecine Translationnelle de Strasbourg (FMTS), Université de Strasbourg, Strasbourg, France – name: h Blood and Marrow Stem Cell Transplant Program, Department of Internal Medicine and The James P. Wilmot Cancer Center, University of Rochester, New York 14642, USA |
| Author_xml | – sequence: 1 givenname: Yannick surname: Dieudonné fullname: Dieudonné, Yannick organization: CNRS UPR 3572 “Immunopathology and Therapeutic Chemistry"/Laboratory of Excellence Medalis, Institute of Molecular and Cellular Biology (IBMC), Strasbourg, France – sequence: 2 givenname: Vincent surname: Gies fullname: Gies, Vincent organization: Laboratoire d'ImmunoRhumatologie Moléculaire, INSERM UMR - S1109, Faculté de Médecine, Fédération Hospitalo-Universitaire OMICARE, Fédération de Médecine Translationnelle de Strasbourg (FMTS), Université de Strasbourg, Strasbourg, France – sequence: 3 givenname: Aurélien surname: Guffroy fullname: Guffroy, Aurélien organization: CNRS UPR 3572 “Immunopathology and Therapeutic Chemistry"/Laboratory of Excellence Medalis, Institute of Molecular and Cellular Biology (IBMC), Strasbourg, France – sequence: 4 givenname: Céline surname: Keime fullname: Keime, Céline organization: IGBMC (Institut de Génétique et de Biologie Moléculaire et Cellulaire), INSERM, U1258, CNRS, UMR7104, Université de Strasbourg, Illkirch, France – sequence: 5 givenname: Anna K. surname: Bird fullname: Bird, Anna K. organization: Department of Medicine, Division of Allergy, Immunology and Rheumatology, University of Rochester Medical Center, Rochester, NY, 14642, USA – sequence: 6 givenname: Jane surname: Liesveld fullname: Liesveld, Jane organization: Blood and Marrow Stem Cell Transplant Program, Department of Internal Medicine and The James P. Wilmot Cancer Center, University of Rochester, New York 14642, USA – sequence: 7 givenname: Jennifer L. surname: Barnas fullname: Barnas, Jennifer L. organization: Department of Medicine, Division of Allergy, Immunology and Rheumatology, University of Rochester Medical Center, Rochester, NY, 14642, USA – sequence: 8 givenname: Vincent surname: Poindron fullname: Poindron, Vincent organization: CNRS UPR 3572 “Immunopathology and Therapeutic Chemistry"/Laboratory of Excellence Medalis, Institute of Molecular and Cellular Biology (IBMC), Strasbourg, France – sequence: 9 givenname: Nawal surname: Douiri fullname: Douiri, Nawal organization: Department of Infectious Diseases, Hôpitaux Universitaires de Strasbourg, Strasbourg, France – sequence: 10 givenname: Pauline surname: Soulas-Sprauel fullname: Soulas-Sprauel, Pauline organization: CNRS UPR 3572 “Immunopathology and Therapeutic Chemistry"/Laboratory of Excellence Medalis, Institute of Molecular and Cellular Biology (IBMC), Strasbourg, France – sequence: 11 givenname: Thierry surname: Martin fullname: Martin, Thierry organization: CNRS UPR 3572 “Immunopathology and Therapeutic Chemistry"/Laboratory of Excellence Medalis, Institute of Molecular and Cellular Biology (IBMC), Strasbourg, France – sequence: 12 givenname: Eric surname: Meffre fullname: Meffre, Eric organization: Departement of Immunobiology, Yale University School of Medicine, New Haven, CT, USA – sequence: 13 givenname: Jennifer H. surname: Anolik fullname: Anolik, Jennifer H. organization: Department of Medicine, Division of Allergy, Immunology and Rheumatology, University of Rochester Medical Center, Rochester, NY, 14642, USA – sequence: 14 givenname: Anne-Sophie surname: Korganow fullname: Korganow, Anne-Sophie email: korganow@unistra.fr organization: CNRS UPR 3572 “Immunopathology and Therapeutic Chemistry"/Laboratory of Excellence Medalis, Institute of Molecular and Cellular Biology (IBMC), Strasbourg, France |
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| Keywords | TLR9 Interferon Systemic lupus erythematosus CD19 Transitional B cells |
| Language | English |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Y.D., V.G., E.M, J.A and A.S.K. wrote the paper. AUTHOR CONTRIBUTIONS Y.D. and V.G. contributed equally to the work. Y.D., V.G., E.M., J.A. and A.S.K. designed the research. Y.D., V.G., A.G., C.K., B.A., L.J., B.J., N.D., V.P, T.M, J.A. and A.S.K. enrolled patients and performed the experiments. Y.D., V.G., A.G., C.K., J.A., E.M., T.M., P.S.S. and A.S.K. analyzed the data. |
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| SubjectTerms | CD19 Cellular Biology Interferon Life Sciences Systemic lupus erythematosus TLR9 Transitional B cells |
| Title | Transitional B cells in quiescent SLE: An early checkpoint imprinted by IFN |
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